Download What is the effect of dung beetles on gastrointestinal nematodes of

What is the effect of dung beetles on gastrointestinal nematodes of stock?
Prepared for the Technical Advisory Group meeting, 18th September 2012, by Simon V. Fowler,
Landcare Research, New Zealand
1. Summary
1/ This review was undertaken because parasitologists have expressed concerns that dung beetles
may increase levels of gastrointestinal nematodes in stock in New Zealand because; i) dung burial
may increase survival of nematodes compared to dung remaining on the pasture surface; ii) large
numbers of infective larvae could then migrate back to the surface in damp soils; iii) overseas studies
cannot be used to inform risk in New Zealand because of differences, particularly in climate.
2/ The review found that most overseas studies comparing dung in the presence or absence of dung
beetles reported substantial reductions in the number of infective 3rd instar larvae of gastrointestinal
nematodes at the soil surface or on pasture foliage.
3/ The break-up of dung on the surface by dung beetles can result in death of the desiccationintolerant 1st /2nd instar nematode larvae, although greater access to oxygen in broken-up dung can
lead to a higher proportion of nematode eggs hatching compared to dung not exposed to beetles.
4/ In most cases, burial of dung by dung beetles appeared to destroy a high proportion of
nematodes, presumably by the processing of dung by the adult beetles. One study showed that
recently buried dung brood balls contained 99.5% less nematode larvae than undisturbed dung pats
remaining on the surface.
5/ Nematode larvae are capable, given moist enough conditions, of migrating back to the surface
from dung buried to 10 cm or sometimes deeper. However, even shallow burial is likely to provide a
hurdle for larval migration when soils do not have high moisture contents, and this hurdle effectively
increases with increased burial depth. Experiments where dung was buried near to artificial barriers
often reported larval migration from depths of 15–20 cm. However, the barriers may be providing
continuous films of moisture encouraging larval migration so need to be interpreted with caution.
6/ The concern that burial of dung by dung beetles could lead to a ‘time bomb’ effect where later
migration to the surface could increase infection of grazing stock, compared with dung remaining
intact on the surface, is a possibility that was not supported by the majority of studies.
7/ Many overseas field studies of the effect of dung beetle activities were conducted in warmer,
more tropical environments than are found in New Zealand, however several key studies do include
periods when the climate match to summers in warmer parts of New Zealand was reasonable. Other
trials were laboratory based and were operated at temperatures that were not excessive compared
to conditions in New Zealand. A few burial trials were conducted outside in temperate areas that
were more directly comparable to most of New Zealand, but none used dung beetles. Overall, the
effect of climate on the interaction between dung beetles, gastrointestinal nematodes and stock reinfection rates are complex, but some overseas studies can be used to predict the likely effect of
dung beetles in at least the warmer regions/seasons in New Zealand.
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8/ More research could be carried out to provide additional information for assessment. However
this is highly unlikely to alter the overall conclusion that in most weather conditions/regions of New
Zealand dung beetle activity will either reduce (or make little difference to) infective larval
nematode numbers available to re-infect stock. It is thus highly unlikely that the action of dung
beetles in New Zealand will increase infection rates of gastrointestinal nematodes of stock.
2. Introduction
The global prevailing view is that dung beetle activity reduces survival of eggs and free-living larvae
of parasitic nematodes, and hence reduces the re-infection rate of stock. However the following
quotes from Vlassoff et al (2001) sum up the issues raised by parasitologists in New Zealand:
“results of studies in New Zealand and overseas have been variable; some beetles reduced larval
numbers while others actually increased them.”
“a risk of dung burial is that remaining viable eggs and larvae may be protected from climatic
extremes and ultraviolet radiation which could enhance their survival”
“if large numbers of L3 are able to survive in soil during periods of drought ... (then this could be) a
potential explanation for the rapid increase in pasture larval counts observed after the first
significant rains in late summer/autumn in some years”
Also in the same review series, Hein et al (2001) commented that:
“Dung burial may not always lead to a reduction in pasture larval burdens. Persistence of soil
moisture in the vicinity of faecal pats may cancel out the reductions achieved in surface larval
numbers and actually encourage later larval migration onto herbage (Bryan 1973).”
The same concerns were raised in Australia before dung beetles were introduced, and were later
considered as minor (Durie in Hughes et al 1975). Durie also gives a useful account of how
nematodes develop in dung and how dung beetle activity could affect this (Hughes et al 1975).
This review has attempted to access all the literature on the effects of dung beetles on the
nematodes that can infect stock as free-living 3rd instar larvae on pasture. Where relevant, studies
that artificially buried dung and measured the effects of this on nematodes have also been included.
Studies are summarised in Table 1 and, where necessary, discussed in more details in the
supplementary material in Appendix 1. This review then addresses the concern that the results of
overseas studies cannot be extrapolated to New Zealand because of differences in climate.
This review does not cover effects of drenches on the activities of dung beetles. These have been
extensively researched, and clearly can have an impact on the possible benefits to be gained from
dung beetle activity in pastoral grazing systems (http://dungbeetle.org.nz/management-practices/).
There are two activities of dung beetles relevant to the potential suppression (or otherwise) of
nematode re-infection rates in stock: firstly the feeding/processing of dung on the surface and the
resulting break-up and possible desiccation of the fresh pat; secondly the burial of dung by beetles.
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Author
Animal
dung
used
Nematode numbers after dung burial/dispersal
Bergstrom
et al 1976
Cattle
&
sheep
Elk
10–20 Aphodius and Canthon spp beetles
exposed to dung for 1–5 days reduced nematode
eggs by 24–90%
1–2 Aphodius beetles per 1g of faeces over 4–36h
reduced larval numbers by 77–92%
48–93% less on foliage
Bergstrom
1983
Bryan 1973
Cattle
Bryan 1976
Cattle
Bryan &
Kerr 1989
Cattle
Chirico et al
2003
Cattle
Coldham
2011
Cattle
English
1979
Horse
40–74% less on foliage, massively less in dung.
99.5% reduction in larval numbers in brood balls cf
surface dung unattacked by beetles.
Infective larvae on grass reduced by 57% (with
minimal beetle activity), 90% (moderate beetle
activity) and 94% (intensive beetle activity)
compared with intact pats
Dung dwelling beetles initially increased L3
numbers in artificial pats (90% RH) over 12 days,
but after another 12 days numbers were much
higher in control pats. Overall, L3 numbers were
2.4x higher in dung without beetles.
Expts carried out in buckets and misted daily with
5 ml of water. Artificial dung burial resulted in 21x
the numbers of nematodes in surface soil cf dung
on surface. In contrast, beetle burial appeared to
destroy nematodes. Where surface dung was kept
wet then nematode numbers were similar from
buried and surface dung treatments. Where
surface dung was not subjected to artificial rain,
nematode numbers were reduced by 86%.
60% reductions in strongylids on grass clippings
from O. gazella in summer period, but beetle
activity curtailed by heavy rain or cooler
temperatures.
Comments
Evidence larval
migration from buried
dung (+/- increased
longevity of larvae)?
n/a
Location, pasture moisture or
rainfall information
n/a
Lab expt: temp 4–24 C (night –
day) on moist filter paper
SE Queensland, trial partly
irrigated. Apr–Jun temperatures
similar to northern NZ summer.
SE Queensland, soil moisture
high at start then declining.
Temperature as for Bryan 1973
Central Queensland. 780mm
rainfall/year. Warmer than NZ.
Low numbers of beetles to simulate numbers seen
in the field in the Tetons, USA
See detailed discussion in Appendix 1
n/a
Indoors – 90% RH and 21°C
Yes – for artificially
buried dung (15 cm
deep). No for dung
buried by beetles (as no
nematodes appeared to
survive).
Indoors parts of trials at 25°C.
Northern Tablelands, NSW.
Annual rainfall 650–1200+ mm
(mostly in summer). Cool
summers (rarely > 32°C) .Winter
snowfalls & frequent frosts (to 10°C)
Increase after 12 days attributed to increased
aeration. Decrease after 24 days could be due to
beetle feeding, dung desiccation or competition with
saprophytic nematodes (arriving on beetles), but
either way beetles overall decreased L3 numbers
Burial rates were low: Onthophagus australis
(50%), O. granulatus (20%), O. gazella (30%)
Artificially buried dung given optimal conditions for
nematode larvae to migrate back to surface (pots
stood in water to guarantee soil was wet). Sampling
by extracting from top 2 cm of soil (no foliage in
pots)
No sign of effect in data
(no later peak in dung
with beetles). However,
author assumed
migration was occurring
as soil moisture levels
were high for entire
period.
Southern Queensland. Rainfall
(av. 1158 mm/yr - described as
regular and prolonged for much of
study plus some periods of heavy
rain noted (e.g. 288 mm in
Feb1976)
Yes, but later peak small
Yes, but later peak small
No
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Lab expt on moist filter paper.
20°C.
See detailed discussion in Appendix 1. Brood ball
data is unique but the massive reduction in larval
numbers was not pointed out by the author.
Study ran from 1975 to 1979
Onthophagus granulatus (native to Australia) in
large numbers but failed to disperse dung.
Introduced O. gazella much more effective but only
in summer. Most nematode infection of horses
occurs in spring/auturm, so additional species
needed if dung beetles to be effective.
Fincher
1973
Cattle
23–54% less in cattle; 75–93% less on foliage
(comparing natural dung beetle levels or
enhanced dung beetle levels with a dung beetle
exclusion treatment)
55–89% less in cattle (treatments as above)
If present, not enough to
interfere with reductions
in larval numbers in
presence of beetles
As above
Coastal Georgia, USA.
1174mm/yr - spread evenly.
Summer mean temperature warm
(July mean max 32°C)
As above
No replication
Fincher
1975
Fincher &
Stewart
1979
Cattle
Cattle
Variable numbers of L3 on grass with dung burial
2.5–10 cm (but no surface check, 1 rep/depth)
Replicated glass tube expt – L3: 89% (2.5cm) and
95% (10cm) reductions cf surface dung.
As above. 37 cm rainfall during
the 16 week experiment. Glass
tube expt indoors at 27°C, 95%
RH.
Comments that glass tubes may have facilitated
migration of larvae from relatively deeply buried
dung because there would be a continuous film of
moisture on the surface of the glass (hence why
some larvae could migrate from depths of 10–15
cm).
Grønvold
1987
Cattle
Earthworms (not dung beetles) excluded from
pats. 50% decrease in Cooperia L3 over late
summer to late spring.
Grønvold et
Cattle
With dung beetles: 88% less larvae in cow pats
(P<0.01); 28% less in 0–6 cm soil (NS); 70%
higher in soil 6–12 cm (NS). 70-90% less by rain
splash.
Houston et
al 1984a
Horse
Mixed results over weekly sampling (4 dates).
Treatments with beetles (22 or 44 pairs) usually
higher than controls (no beetles) but differences
not statistically significant.
Yes. In tube expt,
numbers from surface
dung peaked at 3–4
wks, much lower
numbers from buried
dung peaked at 3–8
wks.
Perhaps a very minor
peak the following
spring, but still about
60% lower than controls.
No (controls without
beetles had same no.
larvae in soil as
treatments where
beetles buried dung –
duration 33 days)
They claim emergence
from buried dung but I
don’t think this is
supported by the data to
any great extent.
Houston et
al 1984b
Horse
Very few L3 migrated onto foliage from burial
depths >5cm (although 1 L3 did emerge from
dung buried to 20 cm)
Hutchinson
et al 1989
Horse
Krecek &
Murrell
1988
Cattle
More larvae in faeces protected from beetles
(numbers per gram – see comments on same trial
in Mfitilodze & Hutchinson 1988). Larval yields on
grass samples were higher with protected faeces,
but differences often not large and varied by year.
n/a
al 1992
Emergence from buried
dung, but not really any
later peak from more
deeply buried dung.
Ostertagia appeared
capable of migrating 15
cm into soil and then
returning to surface
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No replication
Denmark. Substantial rainfall in all
months.
Zimbabwe, >800mm/yr. Warmer
than NZ: average monthly
temperature from 13°C (June) to
20°C (Nov)
Texas. Very low rainfall until 40
mm in one day between sampling
periods 3 and 4 (by which time ¾
of control dung had been
removed!). 5 mm water added
after 2nd sample but not likely to
be enough to penetrate intact
pats. Warmer and drier than NZ.
Watered to saturation once dung
buried. Then sufficient water
provided for plant growth.
College Station, Texas. As above.
Tropical Queensland. Warmer
than NZ. Well-defined summer
wet season.
Foliage and dung samples mixed. Authors thought
more L3 might have emerged from controls if trial
had run longer (but all dung sampled by then!).
Slightly odd expt design as control treatment ended
up with ¾ of dung removed by sampling period 3–4,
whereas in beetle treatments the dung was
dispersed/buried, so less of it would have been
removed for sampling. Makes data hard to interpret.
Beltsville (nr Washington), USA.
Most of trial in Oct/Nov (mean
max 21°C, mean min 10°C).
Rainfall 200mm in Oct/Nov.
30 cm diam. steel cylinders to 5-15 cm: provided an
easy pathway for larvae as suggested by Fincher &
Stewart (1979) for glass tubes? High rainfall fits
with last high no. larvae outside 15 cm cylinder.
Larval migration to grass only occurred in summer
after rains had started (Jan–May).
Lucker
1936
Horse
Percentage recoveries in surface soil of buried
larvae ranged from 0.02–21% (at 2.5cm), 0–3.9%
(at 5–6cm), 0.004–1.9% (at 7.5cm) 0–1.2% (at
10–15cm). Some unquantified recovery from 20
cm burial of horse dung in coarse sand. A range of
soil types used, with reduced recovery from heavy
clay soils.
Percentage recoveries in surface soil from dung
burial in sandy clay loam, sandy loam or coarse
sand were 0.07–8.9% (7–9cm), 0.0009–3.5% (15–
16 cm), 0.0009–0.9% (20–21 cm), 0.0–0.4% (25–
27 cm). Zero recoveries from clay soil.
Lucker
1938
Horse
Mfitilodze &
Hutchinson
1988
Horse
Dung exposed to beetles for 7 days had 20–80%
less infective larvae compared with beetle
excluded dung. Very variable across seasons so
concluded that not epidemiologically significant.
Popay &
Marshall
1996
Sheep
Onthophagus posticus and O. granulatus mostly
reduced larval numbers in dung. (although 1 result
showing significant reverse effect).
Reinecke
1960
Cattle
Waghorn et
al 2002
Sheep
Dung beetle activity encouraged nematode eggs
to hatch but larvae desiccated. Dung beetles
reduced nematode larvae in pats by 99%, and no
increase in larvae in the soil beneath pads. In wet
trials, beetles reduced larvae on foliage by 87%. In
dry trials no significant difference +/- beetles.
Buried dung increased nematode numbers on
foliage in trial 2 (by 88%) but no increase in trial 1.
Greater total numbers in pots from buried dung in
both trials.
Waterhouse
1974
Cattle
48–93% reduction in larvae on pasture
Yes, but substantial
migration to surface only
with shallow burial
Yes. Evidence of ~week
delay in larval recoveries
with deep dung, but
recoveries nearly always
higher for shallow burial
at all sample dates.
Larvae measured in
surface dung not on
grass/soil
No: O. posticus
increased larval no.s in
soil, but no significant
increase on foliage
Yes, but burial only 5cm
(no evidence on
longevity)
Not mentioned
“Precipitation invariably occurred”
in field trials. In laboratory/covered
trials soil was kept moist.
Beltsville (nr Washington, DC).
Mean monthly max 5–31°C, min 5–19, avg annual rain 1110mm.
More continental climate than NZ.
Laboratory study. “Soils were kept
moist at practically all times …
more conducive to the migration
of the infective larvae than would
occur ordinarily in a similar period
in the field”
See Hutchinson et al 1989
NZ. Ruakura.
NW Cape, South Africa “semiarid”. Cool dry winters and hot wet
summers. ‘Wet trials’ – mean max
24–31°C, mean min 11–17°C,
mean daily rainfall 2–15mm
(annual equivalent = 1750mm)
NZ. Rainfall 90 mm (over 28
days), 103 mm (over 34 days)
Not mentioned
Both Lucker 1936 and Lucker 1938 indicate that
“lighter soils, such as fine sandy loam, are most
favourable for vertical migration of horse strongyle
larvae.”
Dung beetles typically will bury to the deep end of
their depth burial range in light soils.
Hutchinson et al 1989 more important as it uses the
same experiment over longer time frame and
includes grass samples. L3 numbers in the dung
turns out to not really matter. However, using
larvae/gram ignores probable large reduction in
total wet weight of beetle affected pats in 7 days
(“faecal pellets were usually completely broken
down to a flattened mass of fibrous debris in 24h”).
Little dung buried/removed. Not clear why O.
granulatus did so little burial (nb this species
ineffective even at high numbers in English (1979).
Foliage sampling was only done on single dates for
each trial, so no tracking through time.
The quantitative results presented here uses the
original data from Reinecke (1960) but re-analyses
it (details in Appendix 1)
Manual dung burial to 5 cm, so no dung beetle
activity (breaking up/processing dung). Sampling
only on one date so no tracking through time. Note
contrast to Coldham (2011) result above where
artificial burial led to survival and migration of larvae
whereas burial by dung beetles didn’t.
Just summarising studies by Bryan (1973, 1976) etc
Table 1. Summarised information from studies of dung beetle activity or dung burial and nematodes used in this review.
5
3. Break-up of dung on the surface and processing/feeding by dung beetles
3.1 Break-up and desiccation of dung
Dung beetles break up the dung on the surface in the process of feeding or creating brood balls. Six
studies show substantial reductions in nematode levels in dung exposed to beetles compared with
dung unexposed to beetles (Bergstrom et al 1976; Bergstrom 1983; Bryan 1976; Chirico et al 2003;
Grønvold et al 1992; Popay & Marshall 1996; Reinecke 1960). However if the broken-up dung on the
pasture surface remains wet enough, and/or conditions are warm enough to result in very rapid
development of the desiccation-resistant 3rd instar larvae, then surface dung could maintain high
levels of nematodes despite some activity by beetles (Coldham 2011; Hutchinson et al 1989). One
study of dung-dwelling beetles (i.e. species that don’t bury dung) showed that the beetles improved
the conditions in a dung pat for development of the infective 3rd instar nematode larvae in the first
12 days, but that larger numbers of larvae were present in the pats without beetles after 24 days –
with overall numbers of 3rd instar larvae being 2.4x higher (Chirico et al 2003). Popay and Marshall
(1996) also had one trial where nematode numbers were significantly higher in surface dung in the
presence of dung beetles. A possible explanation could be that increased levels of oxygen in dung
broken up by beetles led to a higher proportion of nematode eggs hatching (Durie in Hughes 1975;
Reinecke 1960). Greater aeration due to the activity of dung-dwelling beetles was also thought to
explain the higher numbers of 3rd instar larvae after 12 days in the presence of beetles by Chirico et
al (2003). In this study, larval numbers were much higher in control pats after 24 days, giving an
overall decrease in total larval numbers in the presence of beetles of 2.4×.
To summarise, most studies show that dung beetles breaking up dung on the surface decreases
survival of nematodes to the infective L3 stage. However, if conditions are wet enough then
insufficient desiccation could occur and development to the L3 stage might be relatively unaffected
by the surface activities of dung beetles. An increased proportion of nematode eggs could hatch in
dung beetle affected dung because of increased levels of oxygen (required for eggs to hatch)
compared with intact dung pats. In wet conditions it is therefore possible that numbers of eggs
developing to the L3 stage could be increased by the action of dung beetles on surface dung,
although such an effect appears to occur very infrequently. In addition, when such damp conditions
occur, intact dung pats (in the absence of dung beetles) would already be a major source of L3
nematodes, while dung beetles will typically be rapidly burying dung resulting in a proportion of
dung (sometimes high) ending up buried before nematodes can develop to the L3 stage.
3.2 Direct feeding and processing of dung into brood balls
It has been suggested that the feeding action of dung beetles, and their processing of dung into
brood balls for their larvae, could directly reduce the survival of nematode eggs. In particular, Miller
et al (1961) suggested that the grinding action of dung beetle mandibles destroyed nematode eggs.
However, Holter (2002) showed dung beetles filter small particles out of the dung and consume
these rather than doing any chewing. Note that dung beetle larvae do have chewing mouthparts, but
the larvae will only hatch after 3rd instar nematode larvae have matured and possibly left the brood
ball. The Miller et al (1961) result that showed that dung beetle guts did not contain many intact
nematode eggs is still significant in that the beetles themselves would not be capable of transporting
nematode eggs or larvae to any great extent. Despite the critique of Holter (2002) it is still worth
pointing out that in a parallel study with Cryptosporidium oocytes, Mathison & Ditrich (1999)
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showed that only small numbers of oocytes survived passage through the beetle guts. Like Miller
(1961) they concluded that the grinding action of the beetle mouthparts destroyed most of the
oocytes. Again this appears to be unlikely given Holter’s (2002) findings. However, Ryan et al (2011)
then go on to show that dung buried by dung beetles had far fewer oocytes than dung remaining on
the surface. So beetle processing of dung is reducing the survival of Cryptosporidium oocytes by
some means even if the beetles do not chew or grind the dung. Note that Cryptosporidium oocytes
are only 4-6µm in diameter so will be consumed by all the beetle species tested by Holter (2002). As
Nichols et al (2008) points out, we don’t know the mechanism for the destruction of the small
Cryptosporidium spores. It’s quite possible that some of the same destruction could happen with
nematode eggs. Indeed, there is direct evidence of this: Bryan (1976) dug out brood balls three days
after dung beetles had been introduced to fresh dung pats on the ground above. The control dung
pats (no beetles) had approximately 100,000 nematode larvae per 100 g fresh weight of dung. In
contrast, the brood balls had only about 800 nematode larvae per 100 g fresh weight of dung, a
99.5% reduction. Given the three day sampling period, all the nematode larvae would have been 1st
or 2nd instar, so would not yet have migrated from the surface pat or the brood balls. The most
obvious conclusion is that processing of the dung to create the brood ball resulted in the death of
the vast majority of nematode eggs and/or larvae. This is clearly very relevant to the discussion of
the effects of dung beetle burial versus artificial burial experiments (section 4.1, below).
3.3 Studies that don’t distinguish effects of surface activities of dung beetles from dung burial
Several studies report reductions in nematode numbers due to dung beetle activity by measuring
larval numbers on foliage/surface soil (Bryan 1973; Bryan & Kerr 1989; English 1979; Hutchinson et
al 1989; Reinecke 1960; Waterhouse 1974), but cannot distinguish the direct effects of beetles on
dung on the surface with the effects of dung burial. Similarly, Fincher (1973, 1975) show reduction in
infection rates of cattle from beetle activity that could be due to increased surface desiccation of
dung and/or dung burial. Another study also shows a similar reduction in larval nematode numbers
on foliage from earthworm burial of dung (Grønvold 1987).
One study showed dung beetles having no significant effect on nematode numbers on pasture
adjacent to horse dung (Houston et al 1984a), although the number of infective larvae was, at times,
higher in the treatments with beetles than controls. Reinecke (1960) reported that the removal of
small pieces of dung from pats by dung beetles could, under conditions of low rainfall, lead to low
numbers of larval nematodes on grass (whereas the same low levels of rainfall were insufficient to
allow migration of larvae out of intact pats). Hence, under these particular conditions there were
occasions when larval numbers appeared higher in the presence versus the absence of beetles.
However, an analysis of Reinecke’s (1960) data failed to show that this was a statistically significant
effect (Appendix 1). The larval numbers on the grass in these low rainfall trials were extremely small
compared to the larval counts on grass in trials that were conducted in higher rainfall conditions
(Reinecke 1960; data analysed in Appendix 1). In another study (Popay & Marshall 1996), one trial
resulted in an increase in nematode larvae on foliage with dung beetles present compared with
controls, which approached statistical significance (P=0.07). However in the same study, most trials
did not result in an increase in nematodes on foliage in the presence of dung beetles. Finally, a few
studies tracked larval nematode numbers over time and, although there were usually higher
numbers from dung in the absence of beetles at first, there were occasions when a lesser, later peak
occurred in the presence of beetles which was assumed to be due to larval migration from buried
7
dung. In two of these studies (Bryan 1973, 1976) there were examples where, towards the end of
the experiment, there were more larval nematodes on the pasture foliage in the presence of dung
beetles than in their absence. However, the levels were always much lower than the earlier peak
numbers from dung in the absence of beetles. These important findings are discussed in more detail
in the next section on migration of larvae from buried dung.
In summary, most studies using dung beetles show a substantial reduction in nematode larval
numbers in the surface soil or on pasture foliage. Several studies show no statistically significant
effects, and a few show that dung beetle activity can result in a delayed effect where nematode
larvae are assumed to have migrated from buried dung and can give rise to occasions when larval
numbers are higher in the presence rather than the absence of beetles. However, in these examples,
this later peak in larval numbers is always small compared to the numbers of nematode larvae
migrating from dung in the absence of beetles, and there are other issues of data interpretation
discussed in more detail below.
4. Burial of dung and potential migration of nematodes back to the soil surface
Dung beetles bury dung as brood balls in underground chambers for their offspring to feed on. As
sexually immature adults they may also temporarily bury some dung which they feed on over a
period of days. In these burial processes, some dung can end up on the insides of the burrow. The
key question here is whether burial could increase the survival/longevity of nematode eggs and
larvae compared to dung exposed to desiccation and sunlight on the surface, perhaps creating a
‘time bomb’ in the soil if nematode larvae could migrate back to the surface given sufficient
moisture (Coldham 2011; Vlassoff et al 2001; Waghorn et al 2002). Here the evidence for increases
in nematode larvae in soil at depth when dung is buried versus when dung remains on the surface is
reviewed. The question is then asked whether burial depth influences the ability of L3 nematodes to
migrate back to the soil surface and/or on to pasture foliage. Finally the possibility of a delayed
emergence of nematode larvae from buried dung, the so-called ‘time bomb’ effect, is reviewed.
4.1 Does burial of dung increase numbers of nematodes buried in the soil?
Two studies show that nematode numbers were higher in soil after dung beetles had buried dung
compared to the numbers in soil when the dung remained on the surface (Bryan 1976; Popay &
Marshall 1996). However Bryan (1976) also presented data suggesting that 99.5% of nematode
eggs/larvae were destroyed by dung beetles in making brood balls (as described in section 3.2,
above). Two other studies suggest that dung buried by dung beetles has highly reduced numbers of
nematodes. Firstly, Coldham (2011) showed that in moist conditions the same number of nematodes
returned to the soil surface from artificially buried dung compared to moist dung on the surface, but
that burial of dung by dung beetles appeared to result in the destruction of nematodes. Secondly,
Grønvold et al (1992) showed no increase in nematodes in the soil (0-6 cm, 6-12cm, 12-18 cm) when
beetles buried an average of 62% of the dung on the surface (compared with controls i.e. dung on
the surface with no dung beetles).
Although Reinecke (1960) commented that “where rainfall was inadequate to cause larval migration,
the presence of larvae in the soil was probably due to the mechanical removal of dung by beetles” a
8
statistical analysis of the data as part of this review shows no increase of larvae in soil where dung
beetles had been active in either dry or damp conditions (Appendix 1).
One study showed increased nematodes in the soil from artificial burial of dung compared to dung
on the soil surface (Waghorn et al 2002). Lucker (1938) and Persson (1974) record nematodes in soil
after dung had been artificially buried but did not have a surface dung treatment to compare to the
effect of dung burial.
To conclude, artificial burial may increase nematodes in the soil much more dramatically than burial
by dung beetles. In some cases burial by beetles appeared to destroy a high proportion of the
nematodes, presumably by their processing of the dung.
4.2 Effects of burial depth on nematode larval abilities to return to the surface
It has been suggested that shallow buried dung may allow more nematodes to return to the surface
compared with deeper burial. Two New Zealand studies have examples of nematodes returning to
the surface from dung buried artificially to 5 cm (Waghorn et al 2002) and by beetles to generally <5
cm (Popay & Marshall 1996).
Studies that artificially buried dung to a variety of depths typically show a dramatic reduction in the
numbers of nematode larvae migrating to the soil surface and/or foliage with increased burial depth
(Fincher & Stewart 1979; Lucker 1936, 1938). Several studies also report that the presence of
artificial surfaces that would have provided continuous films of water seemed to encourage
migration of nematode larvae from dung buried quite deep e.g. 25 cm in glass tubes in Fincher &
Stewart (1979), or buried wooden boxes in Lucker (1936). Although not mentioned by the authors
this could explain the unusual result of Krecek & Murrell (1988) who had one result where large
numbers of nematodes apparently migrated from surface dung to get past a 15 cm deep steel
barrier and then managed to return to the surface outside the barrier. This issue is discussed further
in Appendix 1. The same effect may also explain the examples of large numbers of 3rd instar larvae
migrating from dung buried as deep as 20 cm by Persson (1974).
To conclude, it is clear that nematode larvae are capable, given moist enough conditions, of
migrating from dung buried to <10 cm or sometimes deeper. However, even shallow burial is likely
to provide a hurdle for larval migration when soils do not have high moisture contents, and this
hurdle effectively increases with increased burial depth. Experiments using artificial barriers that
could provide continuous films of moisture for larval movement need to be interpreted with caution.
4.3 Evidence of delayed migration of L3 from buried dung resulting in a ‘time bomb’ effect?
As mentioned in section 3.3 above, with studies that have extended sampling over time we can ask if
there is a first peak in larval numbers on the surface as expected from direct migration of infective
larvae from surface dung, followed by a second peak in larval numbers from buried dung. This is
particularly well illustrated by data from Bryan (1973). This data has been taken from a graph in the
paper and then re-plotted here as non-cumulative totals per date (Fig 1).
9
500
Number larvae/100g foliage
450
400
350
300
250
control
200
dung beetles
150
100
50
0
0
20
40
60
80
100
120
140
160
Days since pat deposited
Figure 1. The number of 3rd instar larvae of nematodes recovered from pasture foliage adjacent to
artificial dung pats infested with nematode eggs, either in the presence or absence of dung beetles.
Data from cumulative figure in Bryan (1973).
There is a large first peak in larval nematode numbers on foliage (day 30) from direct larval
emergence from surface dung in the absence of dung beetles. There is a second peak when dung
beetles are present (days 50-70) which is thought to be caused by nematode larvae emerging from
buried dung (in this case as a response to a substantial rain event on day 40). Note that the numbers
of nematode larvae are much less than in the first peak, nevertheless between days 50-70 there are
more nematodes on the grass in the dung beetle treatment than in the dung only treatment.
However, this second peak needs to be interpreted with care as the sampling method used removed
all foliage to ground level around each pat on each sampling date. Thus had the grass not been
removed, the numbers of nematode larvae around the control plots would have remained high until
the L3 larvae died (rather than until they were removed by sampling). Presumably this is why Bryan
(1973) presented the data as cumulative numbers. Predicting L3 survival (had they not been
removed by sampling) is not easy, but survival in warm, moist field conditions is typically suggested
to be 10 weeks or more (e.g. Rattray 2003).
In his later study, Bryan (1976) carried out a more detailed experiment where dung pats, brood balls,
soil etc were destructively sampled on four dates. Much of this has been reported above (sections
3.1 to 4.1), but for this section the important difference to Bryan (1973) is that foliage samples were
different radial subsamples around each pat approximately every 10 days, so the earlier sampling
was probably not reducing nematode numbers in the later sampling by overall removal. Thus this
data can be examined non-cumulatively with more confidence. Interestingly, the numbers of
nematode larvae recovered from foliage were nearly always greater around intact pats compared
with pats with dung beetles (see Appendix 1 for details). There was a slightly higher peak at day 84,
right at the end of the experiment, in the treatment with the lowest number of dung beetles. Bryan
(1976) concluded that the small amount of rain that fell had wetted dung that had been shredded by
beetles, and hence encourage nematode larval migration from the shredded dung. However, it was
suggested that the rain was insufficient to wet the intact encrusted pats in the control treatment
that had no dung beetles, so nematodes remained trapped in these larger pats. Bryan (1976)
10
considered that the encrusted control pats would have continued to release larger numbers of
nematodes had there been sufficient rain to wet the intact pat.
Another study shows a delayed, small peak in nematode numbers reaching the surface due to
migration from buried dung, but the numbers were still lower than the numbers migrating on these
dates from intact pats which had had no beetle activity (Fincher 1973). Grønvold (1987) showed the
same pattern with earthworm-buried dung. Finally, Fincher & Stewart (1979) show later peaks of
infective larvae in their glass tube experiment: by week 8, higher levels of infective larvae were being
recorded on the soil surface from dung buried at 7.5 – 10 cm compared with the dung on the surface
treatment (but total numbers emerging from buried dung at these depths for the whole duration of
the trial were only 2.3% of those in the surface dung treatment).
Coldham (2002) specifically set out to test for a ‘time bomb’ effect from dung buried by dung
beetles, but concluded that dung beetle burial destroyed all nematodes. Gronvold et al (1992)
showed a similar effect with dung beetle burial not increasing nematode numbers in soil.
In summary just one study (Bryan 1973), carried out under irrigation, shows that dung beetle burial
can create a situation where higher numbers of nematode larvae are sampled on pasture foliage in
the presence versus the absence of beetles. However, the support for a ‘time bomb’ effect is weak
for two reasons. Firstly, the later peak was far smaller than the earlier peak caused by direct
nematode migration from pats without beetles. Secondly, without the destructive sampling of all the
foliage around the pats on each date it is likely that many larvae would have survived from the first
large peak around the control pats. The sampling in this case was akin to the ‘vacuuming’ of
nematode larvae that can be achieved by use of a different stock type – one of the potential
recommendations for suppressing larval nematode numbers (e.g. Ratray 2003). It’s quite possible
then that in the absence of the sampling, larval nematode numbers would have remained higher in
the controls than in the dung beetle affected pats. This is the pattern revealed in virtually all the
other studies of the potential ‘time bomb’ effect, with the exception of one final, low-level sample in
Bryan (1976). The lack of the ‘time bomb’ effect in most/all studies is probably due to one of more of
the following reasons:
a) Dung beetle feeding/processing of dung destroyed many/all nematodes in buried dung;
b) Buried nematodes can be trapped underground by lack of sufficient moisture in surface soil;
c) Dung was buried too deep for many L3 to return to the surface;
d) Dry dung on the surface still provided enough of a reservoir of desiccation-resistant L3 nematodes
to swamp any later emergence of L3’s from buried dung.
Point (d) is contradictory to the quote from Vlassoff et al (2002) used in the Introduction: “if large
numbers of L3 are able to survive in soil during periods of drought ... (then this could be) a potential
explanation for the rapid increase in pasture larval counts observed after the first significant rains in
late summer/autumn in some years”.
However, point (d) is consistent with an observation by Bryan & Kerr (1989): "Larvae in faecal pats
deposited from July onwards during the 1977 drought survived in large numbers in these pats until
mid-November when rain fell. Then they migrated as a single wave and the resultant pasture
contamination was 10x higher than the usual spring maximum." In this example, faecal pats
deposited in unusual increasingly dry conditions that lasted about 100 days, contributed to the
11
massive peak when the drought broke. It is also likely that as the ground became dry and hard there
would be little burial activity by dung beetles because numbers of beetles typically decrease in
drought conditions and any that were present would be unlikely to be able to bury dung in the hard,
dry soil. Overall, it seems that the presence of dung beetles, either working through or burying dung,
won't enhance the nematode reservoir problem in drought (rather they are likely to offer some
mitigation).
5. Comparing the climates for overseas studies with New Zealand conditions
Where known, comments on the rainfall and temperatures under which overseas studies were
undertaken are given in Table 1. Also noted is whether the study used irrigation. Data are from the
papers where possible, otherwise a Google search was used to find climate data for the area where
the trial was carried out.
Many of the studies in this review were carried out in warmer, more tropical regions than New
Zealand e.g. Bryan (1973, 1976) and English (1979) were conducted in southern Queensland.
However, Bryan (1973, 1976) conducted experiments in autumn (April – June) and it is clear from
climate data that these months typically have temperatures and rainfall similar to parts of New
Zealand over the summer period (Appendix 1). Thus the results of Bryan (1973, 1976) should at least
be pertinent to parts of New Zealand in summer. The same is true for some of the large number of
trials reported by Reinecke (1960), which although conducted in a semi-arid area has some spring
and autumn periods when average temperatures were reasonably similar to the warmer parts of
New Zealand in summer (see Appendix 1). However, several studies were clearly conducted in hotter
weather than New Zealand normally experiences even in summer (Bryan & Kerr 1989; English 1979;
Fincher 1973, 1976; Grønvold et al 1992; Houston et al 1984a, 1984b; Hutchinson et al 1989).
Other trials were laboratory based and were operated at temperatures that were similar to those in
some season/regions of New Zealand (Bergstrom 1983; Bergstrom et al 1976; Coldham 2002; Lucker
1936, 1938). A few dung burial trials were conducted outside in temperate areas that were more
directly comparable to most of New Zealand (Krecek & Murrell 1988; Lucker 1936), but none used
dung beetles. Finally, the trial that tested dung burial by earthworms (Grønvold 1987) was located in
Denmark, in a climate that would be cooler on average than New Zealand.
Regarding moisture levels/rainfall, many trials either had similar amounts of rainfall to areas in New
Zealand in at least some periods (Lucker 1938; Fincher 1973, 1975; Fincher & Stewart 1979;
Grønvold 1987; Grønvold et al 1992; Krecek & Murrell 1988), or supplemented lower rainfall with
irrigation (Bryan 1973). Even Reinecke (1960) in a semi-arid zone only had very low rainfall in winter,
with actually quite substantial rainfall in the warmer months (Appendix 1). Similarly, the study by
Hutchinson et al (1989) was carried out in a dry tropical region of Queensland, but there is a
pronounced summer wet season when most of the 800-1000mm of rain falls. For laboratory trials,
moisture levels were maintained at levels sufficient to allow migration of 3rd instar larvae (Bergstrom
1983; Bergstrom et al 1976; Coldham 2002; Lucker 1936, 1938). In some studies rainfall was clearly
low for substantial periods of the trials (e.g. Bryan 1973, 1976). However, low rainfall for reasonably
long periods of time is quite common in many parts of New Zealand, particularly in summer.
To summarise, although there is considerable overlap in temperatures and rainfall in many studies
with likely conditions in New Zealand pastures, clearly some overseas trials were carried out in a
12
number of climate types that are not found in New Zealand. Overall, overseas trials that examined
the effect of dung beetle activity on nematode larval numbers were conducted in climates that are
warmer on average than most areas of New Zealand. Nevertheless, some of the most detailed
studies (e.g. Bryan 1976; Coldham 2002; Reinecke 1960) do contain trials that were conducted under
environmental conditions that, at least at certain times, would not be unusual in New Zealand.
What effect are some of these differences in weather conditions likely to have on how relevant their
results are for New Zealand? Broadly it seems likely that the effect of the breaking up and
desiccation of dung by beetles (section 3.1, above) will be highly dependent on weather conditions.
As mentioned in section 3.1, cool, moist conditions are likely to reduce the impact of dung break-up
on free-living stages of nematodes. However, it also appears that hot, wet conditions could result in
such a rapid development to the desiccation resistant 3rd instar larval stage that surface dung break
up could also be relatively unimportant. Given that New Zealand does tend to have dry, warm
summers (Rattray 2003) it seems that dung break-up and desiccation from beetle activity could at
least be important for reductions of nematode numbers in summer (or in dry periods in other
seasons). Cool wet winters are likely to lead to prolonged survival of 3rd instar larvae both on the soil
surface and in buried dung (Rattray 2003). In an area with cold damp winters (Denmark), one study
showed that the overwintering surface dung (where earthworms had been excluded) led to higher
numbers of infective larvae on foliage the following spring compared to the pats where dung had
been buried (Grønvold 1987). There are no studies to inform whether the same effect would occur
with dung buried by beetles before a cool wet winter, but the above discussion (sections 3 and 4)
doesn’t present any evidence that the results should be that much different between dung buried by
earthworms or dung beetles. It is also clear that surface dung can be a key reservoir for the
desiccation resistant 3rd instar larvae even after prolonged periods of drought (Bryan & Kerr 1989).
The effect of dung beetle feeding/processing of dung into dung balls on nematode numbers (section
3.2) would not seem to be directly influenced by the weather, but obviously weather influences
levels of beetle activity. Overall, the review of overseas studies on the direct effect of dung beetle
feeding/processing of dung on nematode numbers would seem to be relevant to New Zealand.
The ability of nematode larvae to migrate from buried dung to the soil surface (sections 4.2 and 4.3,
above) will be critically affected by levels of soil moisture and hence rainfall. Soil temperatures per se
are probably relatively unimportant although nematode larvae will survive for longer periods in
cooler temperatures (Rattray 2003). Many studies had adequate moisture for larval migration so the
overall result of this section of the review would seem to be able to be extrapolated to New Zealand.
Overall, the effects of climate on the interaction between dung beetles, gastrointestinal nematodes
and stock re-infection rates are complex. However, there does not seem to be strong evidence from
overseas studies that the typically cool, wet winters and warm, dry summers in New Zealand
(Rattray 2003) will unduly alter the overall conclusion that in most weather conditions dung beetle
activity will tend to reduce larval nematode numbers available to re-infect stock.
6. Acknowledgements
Dan Tompkins, Ian Sutherland and Liz Nichols made helpful comments on earlier versions of this
review.
13
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special reference to their biology and possible methods of prophylaxis. Onderstepoort Journal of
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on numbers and viability of Cryptosporidium oocysts in cattle dung. Experimental Parasitology
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Skipp, R.A., Hay, D.M., Leathwick, D.M., Popay, A.J. 2000. Biological control of gastrointestinal
nematodes of livestock in faeces and pasture. Meat New Zealand Report on Project 96PR36/1.1.
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sheep. New Zealand Veterinary Journal 49, 213–221.
Waghorn, T.S., Leathwick, D.M., Chen, L-Y, Gray, R.A.J., Skipp, R.A. 2002. Influence of
nematophagous fungi, earthworms and dung burial on development of the free-living stages of
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15
Note: The report by Skipp et al (2000) was accessed but contains the same information as Waghorn
et al (2002) and Popay & Marshall (1996).
8. Appendix 1: supplementary information
Bryan 1973 and Bryan 1976 are important studies, so were reviewed in detail in the main text. The
re-plotted data from Bryan 1976 are shown in Figure 1 in section 4.3. Data were also extracted from
Bryan (1976) and re-plotted here (Figure 2). Bryan 1976 is the only study found that measured larval
nematode numbers in brood balls. Data from the histograms in Bryan (1976) have been extracted
and presented in Table 2. Dung burial by beetles does result in nematode larvae in the brood balls,
however the numbers are dramatically reduced compared with dung remaining on the surface
(Table 2).
pat
2 beetles
10 beetles
30 beetles
Mean
% reduction
day 3
100000
*
300
800
550
99.5%
day 8
24938
900
220
320
480
98.1%
day 18
590
150
550
180
293.3
50.3%
day 84
750
150
300
30
160
78.7%
Table 2. The numbers of nematode larvae (per 100g dung) in the control pats (no dung beetles)
versus brood balls dug out of the ground in the three dung beetle treatments. The mean numbers of
larvae in the brood balls on each sampling date were used to calculate the percentage reduction
versus numbers in the control pat. The most important comparison is at day 3 because no larvae
would have reached the potentially migratory 3rd instar stage. This 99.5% reduction is presumably
caused by the dung beetle burying activity which probably aerates and desiccates the dung (which
will kill 1st and 2nd instar larvae) but also perhaps due to the processing of the dung by the specialised
filtering mouthparts of the adult beetles. *No dung balls by day 3 in the 2-beetle treatments
16
Figure 2. Numbers of 3rd instar larvae recovered from pasture foliage. Data extracted from
cumulative graph in Bryan (1976) and re-plotted non-cumulatively. Control pads had no dung
beetles. Moderate rainfall events occurred early in the trial and also on days 14 and 53 (just
preceding the two main peaks of larval migration). There was only 1 sampling date (day 84) when
larval recoveries were substantially higher in one of the dung beetle treatments versus the controls
(see main text, section 4.3, for the author’s explanation).
Although these studies were located at Glenlogan Field Station in SE Queensland, because they ran
from April-June, the mean monthly temperatures and rainfall were a reasonable match for a
northern NZ summer (Table 3).
Whangarei – temperatures
Whangarei - rainfall
Napier - temperatures
Napier - rainfall
Glenlogan temperatures
Glenlogan - rainfall
January
24.4/15.4
90
24.4/14.6
48
April
26.9/14.2
75.8
February
24.2/15.4
112
24.1/14.5
62
May
23.8/10.9
78.5
March
23.0/15.0
142
22.6/12.8
85
June
21.3/6.8
40.3
Table 3. Mean monthly maximum and minimum temperature for the warmest summer months in
Whangarei and Napier, compared with the experimental period (April-June) at Glenlogan Field
Station, the field site for trials reported in Bryan (1973, 1976).
The Glenlogan Field Station climate data were obtained from:
http://weather.ninemsn.com.au/climate/station.jsp?lt=site&lc=40454
New Zealand climate data were obtained from:
https://en.wikipedia.org/wiki/Whangarei
http://en.wikipedia.org/wiki/Napier,_New_Zealand
Houston et al 1984b
Mean number of L3 on
foliage
The data from this paper were plotted to illustrate the effect of burial depth more clearly (Fig. 3).
150
100
50
0
0
10
20
30
40
Burial depth of dung (cm)
Figure 3. The numbers of 3rd instar larvae migrating onto pasture foliage from dung artificially buried
to various depths.
17
Hutchinson et al (1989) and Mfitilodze & Hutchinson (1988) show reductions in 3rd instar larvae of
horse strongyloids in dung open to dung beetles compared with dung protected from beetles for 7
days. They claim these are minor, although this might underestimate the differences because
numbers were expressed per gram wet weight of dung. Hence they assume that dung beetle activity
(which they say shredded dung within 24h) didn’t reduce the total weight of the 1 kg artificial dung
pat versus dung pats protected from beetles. However, Hutchinson et al (1989) went on to measure
larvae on the grass surrounding the pats after 7 days and then at monthly intervals. They found that
numbers of infective larvae were slightly higher on average on grass around pats protected from
dung beetles, but numbers were quite variable over time, with no clear pattern, suggesting the dung
beetle processing horse dung would be epidemiologically insignificant for strongyloids in this system.
However dung beetles do not show any indication of making the situation worse. It seems that the
eggs develop to the L3 stage so rapidly in the hot, wet summer conditions that the action of beetles
dispersing the dung is not effective at killing larvae in the first two instars. At other times of the year,
conditions are usually so dry that the larvae cannot migrate from the dung to the grass anyway.
Krecek & Murrell (1988) used buried barriers in the form of 30 cm diameter steel tubes to show that
large numbers of nematode larvae could migrate from surface dung to at least 15 cm deep and then
return to the surface outside the barrier. This result seems unusual in two respects. Firstly the
numbers of nematodes migrating around the 15 cm deep barrier in particular is large compared with
other studies above. Secondly most studies do not report nematodes penetrating soil very deeply
without dung burial (e.g. Popay and Marshall 1996). It seems possible that barriers might encourage
nematode movement in a similar way as Fincher & Stewart (1979) suggest for their glass tube
experiment, and Lucker 1938 suggests for experiments with wooden barriers i.e. the damp barrier
provides an easy route for larval travel. In Krecek and Murrell (1988) larval movement may also have
been exacerbated by the heavy rain they report in the latter part of their trial: it may be that
nematode larvae were virtually ‘washed’ down the inside of the steel cylinders. Bryan (1973) also
makes the comment that heavy rain can wash nematode larvae deep into soil, although presents no
data on this.
Percentage of larvae reaching
surface
Lucker (1936, 1938) showed few nematode larvae reached the soil surface from burial depths of >10
cm (Figure 4).
25
20
15
Heavy clay soil
10
Sandy/clay loam
Light sandy loam
5
Sand
0
0
10
20
30
Burial depth (cm)
18
Figure 4. The percentage of 3rd instar larvae migrating to the soil surface from either direct burial of
3rd instar larvae (Lucker 1936) or burial of dung infested with known quantities of nematode eggs or
larvae (Lucker 1938).
Reinecke (1960) is a huge study and presents a large amount of data, but as published is difficult to
follow. The data were re-evaluated here.
Larval nematode numbers in pat (log n+1)
Of the 58 trials - only some had dung beetle activity. Trials were excluded if Reinecke’s (1960)
comments made it clear that atmospheric conditions were unsuitable for nematode larval
development, or the trial ran for an unusually long time, or there were other unusual circumstance
(e.g. a dripping trough in one trial; no grass near pad in another). Dung beetle activity was scored as
0 (no mention), 1 (dung beetle activity mentioned) and 2 (major impact mentioned). Firstly, the
number of nematode larvae in the dung pats was examined in relation to dung beetle activity across
both dry and wet trials (as dung beetles were active in both). Dung beetle activity clearly reduced
the number of nematode larvae in dung pats (Fig 5). The mean number of larvae collected from
unattacked pads (back-transformed mean) was 1308.8 and from pads affected by dung beetles
(activity levels 1+2 grouped) was 12.9, a reduction of 99.0%.
6
5
4
3
2
1
0
0
1
2
Dung beetle activity score
Figure 5. The total number of nematode larvae in dung pats with levels of dung beetle activity scored
as 0, 1 or 2 (see text for details). Y = -1.23X + 3.02, F 1,38 = 28.76, P<0.00001, r2 = 0.42.
Soil under intact pats with no beetle activity also had slightly more nematode larvae than soil under
pats where beetles had been active, but the effect was not statistically significant.
Trials were then divided into those where Reinecke (1960) considered that insufficient rain had
fallen to enable nematode larvae to migrate from dung pats, and those where rainfall was sufficient.
In trials where sufficient rain fell to allow migration of 3rd instar larvae out of the dung pads, there
19
were more larvae recovered from adjacent pasture foliage around pads with no beetles than pads
with beetle activity levels of 1 or 2 (grouped here because only 1 trial with sufficient rain had a
beetle activity score of 2). Back-transformed means (180.8 and 22.8 for beetle activity levels of 0 and
1+2) reveal that this is a percentage reduction of 87.4% (Fig 6).
Larval nematode numbers on foliage
(log n+1)
3
2.5
2
1.5
1
0.5
0
0
1/2
Dung beetle activity score
Figure 6. The total number of 3rd instar larvae recovered from pasture foliage adjacent to dung pats
where dung beetles had not been active (0) or had been moderately or highly active (1/2), in trials
where sufficient rain had fallen to allow migration of larvae away from the dung pat. The difference
is statistically significant (t13 = 2.99, P<0.05). Error bars SEM.
Reinecke (1960) reported that in trials where insufficient rain fell to enable larval migration away
from the dung pat itself, then smaller amounts of rain could allow migration from small pieces of
dung left behind after dung beetle activity. The re-analysed data do show some evidence that this is
happening because in dry conditions there were more nematode larvae recovered on adjacent
foliage in the trials that had moderate dung beetle activity (Fig 7), but the effect was not statistically
significant. Note that the mean numbers of larvae recovered from these dry trials are much lower
than from the moist trials (means of 1.5, 5.1 and 0.9 for dung beetle activity scores of 0, 1 and 2
versus means in moist conditions of 180.8 and 22.8 for beetle activity levels of 0 and 1+2).
20
Larval nematode numbers on foliage
(log n+1)
1.2
1
0.8
0.6
0.4
0.2
0
0
1
2
Dung beetle activity score
Figure 7. The total number of 3rd instar larvae recovered from pasture foliage adjacent to dung pats
where dung beetles had not been active (0) or had been moderately (1) or highly active (2), in trials
where insufficient rain had fallen to allow migration of larvae away from the dung pat. The
difference between activity levels 0 and 1 is not statistically significant (t11 = 1.49, P>0.1). Error bars
SEM.
Similar analyses of the number of nematodes recovered from soil under the pat, adjacent soil or
from plant roots, revealed no significant differences regardless of whether dry and moist trials were
analysed together or separately.
Climate data for Reinecke (1960) used in Table 1 were obtained from the nearby city of Vryburg:
http://www.saexplorer.co.za/south-africa/climate/vryburg_climate.asp
Persson 1974 presents data on several artificial burial trials. This has been summarised here in a
simple table (Table 4).
Date
Depth
No eggs
15/10/1971
15/10/1971
15/10/1971
15/10/1971
9/05/1972
9/05/1972
9/05/1972
9/05/1972
10
20
10
20
10
20
10
20
180000
180000
No L3
20000
20000
180000
180000
15000
15000
total recoveries
moss soil clay soil
10
16
308
291
539
97
722
663
Table 4. Data tabulated from Persson (1974).
21
13
18
135
665
679
307
1010
247
sandy
soil
31
2
345
278
114
33
52
12
54
36
788
1234
1332
437
1784
922
There was no obvious pattern of decreased emergence of larvae with increased burial depth. This is
unusual compared to other burial studies. The design is similar to the Krecek and Murrell (1988)
experiment with aluminium cylinders. Thus the same concern exists, that 3rd instar larval nematodes
could be travelling up the inside of the metal cylinders as in other experiments using barriers.
Popay & Marshall 2002
This New Zealand study shows that shallow (less than 5 cm) burial of dung by the small Australian
beetle Onthophagous granulatus results in higher nematode larval numbers in the soil, but there
was no significant increase in the numbers of larvae on foliage. The study has not been published in
a peer reviewed journal, and does contain several unusual techniques/results e.g. covering
containers with cling-film in one trial that resulted in high levels of fungal infection on the dung. The
trials also used two marsupial-adapted, adventive dung beetles that do normally process much stock
dung in New Zealand. In their report they mention a further set of trials but no details are given.
Waghorn et al 2002
This New Zealand experiment used shallow, artificial burial of dung to 5 cm to simulate dung beetle
burial activities. Notably it is one of the only experiments to ever show that dung burial can lead to a
significant increase in the numbers of 3rd instar larvae on foliage when compared to the control
treatment with dung exposed on the surface.
22